Skip to main content
Top
Published in: Cancer and Metastasis Reviews 1/2023

Open Access 06-01-2023 | Prostate Cancer

Liquid biopsy for monitoring of tumor dormancy and early detection of disease recurrence in solid tumors

Authors: Isabel Heidrich, Benjamin Deitert, Stefan Werner, Klaus Pantel

Published in: Cancer and Metastasis Reviews | Issue 1/2023

Login to get access

Abstract

Cancer is one of the three leading causes of death worldwide. Even after successful therapy and achieving remission, the risk of relapse often remains. In this context, dormant residual cancer cells in secondary organs such as the bone marrow constitute the cellular reservoir from which late tumor recurrences arise. This dilemma leads the term of minimal residual disease, which reflects the presence of tumor cells disseminated from the primary lesion to distant organs in patients who lack any clinical or radiological signs of metastasis or residual tumor cells left behind after therapy that eventually lead to local recurrence. Disseminated tumor cells have the ability to survive in a dormant state following treatment and linger unrecognized for more than a decade before emerging as recurrent disease. They are able to breakup their dormant state and to readopt their proliferation under certain circumstances, which can finally lead to distant relapse and cancer-associated death. In recent years, extensive molecular and genetic characterization of disseminated tumor cells and blood-based biomarker has contributed significantly to our understanding of the frequency and prevalence of tumor dormancy. In this article, we describe the clinical relevance of disseminated tumor cells and highlight how latest advances in different liquid biopsy approaches can be used to detect, characterize, and monitor minimal residual disease in breast cancer, prostate cancer, and melanoma patients.
Literature
45.
go back to reference Wild, C. P., & W. E., Stewart BW, (Eds.). (2020). World cancer report: Cancer Research for Cancer Prevention. Lyon, France: International Agency for Research on Cancer. Wild, C. P., & W. E., Stewart BW, (Eds.). (2020). World cancer report: Cancer Research for Cancer Prevention. Lyon, France: International Agency for Research on Cancer.
46.
48.
go back to reference Smith, G. L. (2014). The long and short of tamoxifen therapy: A review of the ATLAS Trial. Journal of the Advanced Practitioner in Oncology, 5(1), 57–60.PubMedPubMedCentral Smith, G. L. (2014). The long and short of tamoxifen therapy: A review of the ATLAS Trial. Journal of the Advanced Practitioner in Oncology, 5(1), 57–60.PubMedPubMedCentral
49.
go back to reference Early Breast Cancer Trialists’ Collaborative, G, Davies, C., Godwin, J., Gray, R., Clarke, M., Cutter, D., et al. (2011). Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet, 378(9793), 771–784. https://doi.org/10.1016/S0140-6736(11)60993-8CrossRef Early Breast Cancer Trialists’ Collaborative, G, Davies, C., Godwin, J., Gray, R., Clarke, M., Cutter, D., et al. (2011). Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet, 378(9793), 771–784. https://​doi.​org/​10.​1016/​S0140-6736(11)60993-8CrossRef
56.
go back to reference Baselga, J., Semiglazov, V., van Dam, P., Manikhas, A., Bellet, M., Mayordomo, J., et al. (2009). Phase II randomized study of neoadjuvant everolimus plus letrozole compared with placebo plus letrozole in patients with estrogen receptor-positive breast cancer. Journal of Clinical Oncology, 27(16), 2630–2637. https://doi.org/10.1200/JCO.2008.18.8391CrossRefPubMed Baselga, J., Semiglazov, V., van Dam, P., Manikhas, A., Bellet, M., Mayordomo, J., et al. (2009). Phase II randomized study of neoadjuvant everolimus plus letrozole compared with placebo plus letrozole in patients with estrogen receptor-positive breast cancer. Journal of Clinical Oncology, 27(16), 2630–2637. https://​doi.​org/​10.​1200/​JCO.​2008.​18.​8391CrossRefPubMed
61.
go back to reference Hartkopf, A. D., Banys, M., Meier-Stiegen, F., Hahn, M., Rohm, C., Hoffmann, J., et al. (2013). The HER2 status of disseminated tumor cells in the bone marrow of early breast cancer patients is independent from primary tumor and predicts higher risk of relapse. Breast Cancer Research and Treatment, 138(2), 509–517. https://doi.org/10.1007/s10549-013-2470-9CrossRefPubMed Hartkopf, A. D., Banys, M., Meier-Stiegen, F., Hahn, M., Rohm, C., Hoffmann, J., et al. (2013). The HER2 status of disseminated tumor cells in the bone marrow of early breast cancer patients is independent from primary tumor and predicts higher risk of relapse. Breast Cancer Research and Treatment, 138(2), 509–517. https://​doi.​org/​10.​1007/​s10549-013-2470-9CrossRefPubMed
62.
71.
go back to reference Lauro, S., Trasatti, L., Bordin, F., Lanzetta, G., Bria, E., Gelibter, A., et al. (1999). Comparison of CEA, MCA, CA 15–3 and CA 27–29 in follow-up and monitoring therapeutic response in breast cancer patients. Anticancer Research, 19(4C), 3511–3515.PubMed Lauro, S., Trasatti, L., Bordin, F., Lanzetta, G., Bria, E., Gelibter, A., et al. (1999). Comparison of CEA, MCA, CA 15–3 and CA 27–29 in follow-up and monitoring therapeutic response in breast cancer patients. Anticancer Research, 19(4C), 3511–3515.PubMed
72.
go back to reference Rack, B., Schindlbeck, C., Juckstock, J., Andergassen, U., Hepp, P., Zwingers, T., et al. (2014). Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst, 106(5), https://doi.org/10.1093/jnci/dju066 Rack, B., Schindlbeck, C., Juckstock, J., Andergassen, U., Hepp, P., Zwingers, T., et al. (2014). Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst, 106(5), https://​doi.​org/​10.​1093/​jnci/​dju066
73.
go back to reference Pierga, J. Y., Bidard, F. C., Mathiot, C., Brain, E., Delaloge, S., Giachetti, S., et al. (2008). Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clinical Cancer Research, 14(21), 7004–7010. https://doi.org/10.1158/1078-0432.CCR-08-0030CrossRefPubMed Pierga, J. Y., Bidard, F. C., Mathiot, C., Brain, E., Delaloge, S., Giachetti, S., et al. (2008). Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clinical Cancer Research, 14(21), 7004–7010. https://​doi.​org/​10.​1158/​1078-0432.​CCR-08-0030CrossRefPubMed
76.
94.
go back to reference Oberneder, R., Riesenberg, R., Kriegmair, M., Bitzer, U., Klammert, R., Schneede, P., et al. (1994). Immunocytochemical detection and phenotypic characterization of micrometastatic tumour cells in bone marrow of patients with prostate cancer. Urological Research, 22(1), 3–8. https://doi.org/10.1007/BF00431541CrossRefPubMed Oberneder, R., Riesenberg, R., Kriegmair, M., Bitzer, U., Klammert, R., Schneede, P., et al. (1994). Immunocytochemical detection and phenotypic characterization of micrometastatic tumour cells in bone marrow of patients with prostate cancer. Urological Research, 22(1), 3–8. https://​doi.​org/​10.​1007/​BF00431541CrossRefPubMed
97.
go back to reference Mueller, P., Carroll, P., Bowers, E., Moore, D., 2nd., Cher, M., Presti, J., et al. (1998). Low frequency epithelial cells in bone marrow aspirates from prostate carcinoma patients are cytogenetically aberrant. Cancer, 83(3), 538–546.CrossRefPubMed Mueller, P., Carroll, P., Bowers, E., Moore, D., 2nd., Cher, M., Presti, J., et al. (1998). Low frequency epithelial cells in bone marrow aspirates from prostate carcinoma patients are cytogenetically aberrant. Cancer, 83(3), 538–546.CrossRefPubMed
101.
go back to reference Berg, A., Berner, A., Lilleby, W., Bruland, O. S., Fossa, S. D., Nesland, J. M., et al. (2007). Impact of disseminated tumor cells in bone marrow at diagnosis in patients with nonmetastatic prostate cancer treated by definitive radiotherapy. International Journal of Cancer, 120(8), 1603–1609. https://doi.org/10.1002/ijc.22488CrossRefPubMed Berg, A., Berner, A., Lilleby, W., Bruland, O. S., Fossa, S. D., Nesland, J. M., et al. (2007). Impact of disseminated tumor cells in bone marrow at diagnosis in patients with nonmetastatic prostate cancer treated by definitive radiotherapy. International Journal of Cancer, 120(8), 1603–1609. https://​doi.​org/​10.​1002/​ijc.​22488CrossRefPubMed
102.
106.
go back to reference Todenhofer, T., Hennenlotter, J., Faber, F., Wallwiener, D., Schilling, D., Kuhs, U., et al. (2015). Significance of apoptotic and non-apoptotic disseminated tumor cells in the bone marrow of patients with clinically localized prostate cancer. Prostate, 75(6), 637–645. https://doi.org/10.1002/pros.22947CrossRefPubMed Todenhofer, T., Hennenlotter, J., Faber, F., Wallwiener, D., Schilling, D., Kuhs, U., et al. (2015). Significance of apoptotic and non-apoptotic disseminated tumor cells in the bone marrow of patients with clinically localized prostate cancer. Prostate, 75(6), 637–645. https://​doi.​org/​10.​1002/​pros.​22947CrossRefPubMed
108.
go back to reference Chalfin, H. J., Glavaris, S. A., Malihi, P. D., Sperger, J. M., Gorin, M. A., Lu, C., et al. (2018). Prostate cancer disseminated tumor cells are rarely detected in the bone marrow of patients with localized disease undergoing radical prostatectomy across multiple rare cell detection platforms. Journal of Urology, 199(6), 1494–1501. https://doi.org/10.1016/j.juro.2018.01.033CrossRefPubMed Chalfin, H. J., Glavaris, S. A., Malihi, P. D., Sperger, J. M., Gorin, M. A., Lu, C., et al. (2018). Prostate cancer disseminated tumor cells are rarely detected in the bone marrow of patients with localized disease undergoing radical prostatectomy across multiple rare cell detection platforms. Journal of Urology, 199(6), 1494–1501. https://​doi.​org/​10.​1016/​j.​juro.​2018.​01.​033CrossRefPubMed
115.
116.
go back to reference Budna-Tukan, J., Swierczewska, M., Mazel, M., Cieslikowski, W. A., Ida, A., Jankowiak, A., et al. (2019). Analysis of circulating tumor cells in patients with non-metastatic high-risk prostate cancer before and after radiotherapy using three different enumeration assays. Cancers (Basel), 11(6), 802. https://doi.org/10.3390/cancers11060802CrossRefPubMed Budna-Tukan, J., Swierczewska, M., Mazel, M., Cieslikowski, W. A., Ida, A., Jankowiak, A., et al. (2019). Analysis of circulating tumor cells in patients with non-metastatic high-risk prostate cancer before and after radiotherapy using three different enumeration assays. Cancers (Basel), 11(6), 802. https://​doi.​org/​10.​3390/​cancers11060802CrossRefPubMed
133.
136.
go back to reference Yousaf, A., Tjien-Fooh, F. J., Rentroia-Pacheco, B., Quattrocchi, E., Kobic, A., Tempel, D., et al. (2021). Validation of CP-GEP (Merlin Assay) for predicting sentinel lymph node metastasis in primary cutaneous melanoma patients: a U.S. cohort study. Intenational Journal of Dermatology, 60(7), 851–856. https://doi.org/10.1111/ijd.15594CrossRef Yousaf, A., Tjien-Fooh, F. J., Rentroia-Pacheco, B., Quattrocchi, E., Kobic, A., Tempel, D., et al. (2021). Validation of CP-GEP (Merlin Assay) for predicting sentinel lymph node metastasis in primary cutaneous melanoma patients: a U.S. cohort study. Intenational Journal of Dermatology, 60(7), 851–856. https://​doi.​org/​10.​1111/​ijd.​15594CrossRef
142.
go back to reference Gutzmer, R., Stroyakovskiy, D., Gogas, H., Robert, C., Lewis, K., Protsenko, S., et al. (2020). Atezolizumab, vemurafenib, and cobimetinib as first-line treatment for unresectable advanced BRAF(V600) mutation-positive melanoma (IMspire150): Primary analysis of the randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 395(10240), 1835–1844. https://doi.org/10.1016/S0140-6736(20)30934-XCrossRefPubMed Gutzmer, R., Stroyakovskiy, D., Gogas, H., Robert, C., Lewis, K., Protsenko, S., et al. (2020). Atezolizumab, vemurafenib, and cobimetinib as first-line treatment for unresectable advanced BRAF(V600) mutation-positive melanoma (IMspire150): Primary analysis of the randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 395(10240), 1835–1844. https://​doi.​org/​10.​1016/​S0140-6736(20)30934-XCrossRefPubMed
158.
161.
go back to reference Papadaki, M. A., Stoupis, G., Theodoropoulos, P. A., Mavroudis, D., Georgoulias, V., & Agelaki, S. (2019). Circulating tumor cells with stemness and epithelial-to-mesenchymal transition features are chemoresistant and predictive of poor outcome in metastatic breast cancer. Molecular Cancer Therapeutics, 18(2), 437–447. https://doi.org/10.1158/1535-7163.MCT-18-0584CrossRefPubMed Papadaki, M. A., Stoupis, G., Theodoropoulos, P. A., Mavroudis, D., Georgoulias, V., & Agelaki, S. (2019). Circulating tumor cells with stemness and epithelial-to-mesenchymal transition features are chemoresistant and predictive of poor outcome in metastatic breast cancer. Molecular Cancer Therapeutics, 18(2), 437–447. https://​doi.​org/​10.​1158/​1535-7163.​MCT-18-0584CrossRefPubMed
162.
go back to reference Ascierto, P. A., Del Vecchio, M., Mandala, M., Gogas, H., Arance, A. M., Dalle, S., et al. (2020). Adjuvant nivolumab versus ipilimumab in resected stage IIIB-C and stage IV melanoma (CheckMate 238): 4-year results from a multicentre, double-blind, randomised, controlled, phase 3 trial. The lancet Oncology, 21(11), 1465–1477. https://doi.org/10.1016/S1470-2045(20)30494-0CrossRefPubMed Ascierto, P. A., Del Vecchio, M., Mandala, M., Gogas, H., Arance, A. M., Dalle, S., et al. (2020). Adjuvant nivolumab versus ipilimumab in resected stage IIIB-C and stage IV melanoma (CheckMate 238): 4-year results from a multicentre, double-blind, randomised, controlled, phase 3 trial. The lancet Oncology, 21(11), 1465–1477. https://​doi.​org/​10.​1016/​S1470-2045(20)30494-0CrossRefPubMed
163.
go back to reference Dummer, R., Brase, J. C., Garrett, J., Campbell, C. D., Gasal, E., Squires, M., et al. (2020). Adjuvant dabrafenib plus trametinib versus placebo in patients with resected, BRAF(V600)-mutant, stage III melanoma (COMBI-AD): Exploratory biomarker analyses from a randomised, phase 3 trial. The lancet Oncology, 21(3), 358–372. https://doi.org/10.1016/S1470-2045(20)30062-0CrossRefPubMed Dummer, R., Brase, J. C., Garrett, J., Campbell, C. D., Gasal, E., Squires, M., et al. (2020). Adjuvant dabrafenib plus trametinib versus placebo in patients with resected, BRAF(V600)-mutant, stage III melanoma (COMBI-AD): Exploratory biomarker analyses from a randomised, phase 3 trial. The lancet Oncology, 21(3), 358–372. https://​doi.​org/​10.​1016/​S1470-2045(20)30062-0CrossRefPubMed
164.
go back to reference Lampignano, R., Neumann, M., Weber, S., Kloten, V., Herdean, A., Voss, T., Groelz, D., Babayan, A., Tibbesma, M., Schlumpberger, M., Chemi, F., Rothwell, D. G., Wikman, H., Galizzi, J. P., Riise Bergheim, I., Russnes, H., Mussolin, B., Bonin, S., Voigt, C., Musa, H., … Heitzer, E. (2020). Multicenter evaluation of circulating cell-free DNA extraction and downstream analyses for the development of standardized (pre)analytical work flows. Clinical Chemistry, 66(1), 149–160. https://doi.org/10.1373/clinchem.2019.306837 Lampignano, R., Neumann, M., Weber, S., Kloten, V., Herdean, A., Voss, T., Groelz, D., Babayan, A., Tibbesma, M., Schlumpberger, M., Chemi, F., Rothwell, D. G., Wikman, H., Galizzi, J. P., Riise Bergheim, I., Russnes, H., Mussolin, B., Bonin, S., Voigt, C., Musa, H., … Heitzer, E. (2020). Multicenter evaluation of circulating cell-free DNA extraction and downstream analyses for the development of standardized (pre)analytical work flows. Clinical Chemistry66(1), 149–160. https://​doi.​org/​10.​1373/​clinchem.​2019.​306837
Metadata
Title
Liquid biopsy for monitoring of tumor dormancy and early detection of disease recurrence in solid tumors
Authors
Isabel Heidrich
Benjamin Deitert
Stefan Werner
Klaus Pantel
Publication date
06-01-2023
Publisher
Springer US
Published in
Cancer and Metastasis Reviews / Issue 1/2023
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-022-10075-x

Other articles of this Issue 1/2023

Cancer and Metastasis Reviews 1/2023 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine